Makorin 1 controls embryonic patterning by alleviating Bruno1-mediated repression of oskar translation.
Makorins are evolutionary conserved proteins that contain C3H-type zinc finger modules and a RING E3 ubiquitin ligase domain. In Drosophila, maternal Makorin 1 (Mkrn1) has been linked to embryonic patterning but the mechanism remained unsolved. Here, we show that Mkrn1 is essential for axis specific...
Main Authors: | , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Public Library of Science (PLoS)
2020-01-01
|
Series: | PLoS Genetics |
Online Access: | https://doi.org/10.1371/journal.pgen.1008581 |
id |
doaj-f269777d24fd405bb6f2a90e862f6c95 |
---|---|
record_format |
Article |
spelling |
doaj-f269777d24fd405bb6f2a90e862f6c952021-04-21T13:51:34ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042020-01-01161e100858110.1371/journal.pgen.1008581Makorin 1 controls embryonic patterning by alleviating Bruno1-mediated repression of oskar translation.Annabelle DoldHong HanNiankun LiuAndrea HildebrandtMirko BrüggemannCornelia RückléHeike HänelAnke BuschPetra BeliKathi ZarnackJulian KönigJean-Yves RoignantPaul LaskoMakorins are evolutionary conserved proteins that contain C3H-type zinc finger modules and a RING E3 ubiquitin ligase domain. In Drosophila, maternal Makorin 1 (Mkrn1) has been linked to embryonic patterning but the mechanism remained unsolved. Here, we show that Mkrn1 is essential for axis specification and pole plasm assembly by translational activation of oskar (osk). We demonstrate that Mkrn1 interacts with poly(A) binding protein (pAbp) and binds specifically to osk 3' UTR in a region adjacent to A-rich sequences. Using Drosophila S2R+ cultured cells we show that this binding site overlaps with a Bruno1 (Bru1) responsive element (BREs) that regulates osk translation. We observe increased association of the translational repressor Bru1 with osk mRNA upon depletion of Mkrn1, indicating that both proteins compete for osk binding. Consistently, reducing Bru1 dosage partially rescues viability and Osk protein level in ovaries from Mkrn1 females. We conclude that Mkrn1 controls embryonic patterning and germ cell formation by specifically activating osk translation, most likely by competing with Bru1 to bind to osk 3' UTR.https://doi.org/10.1371/journal.pgen.1008581 |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Annabelle Dold Hong Han Niankun Liu Andrea Hildebrandt Mirko Brüggemann Cornelia Rücklé Heike Hänel Anke Busch Petra Beli Kathi Zarnack Julian König Jean-Yves Roignant Paul Lasko |
spellingShingle |
Annabelle Dold Hong Han Niankun Liu Andrea Hildebrandt Mirko Brüggemann Cornelia Rücklé Heike Hänel Anke Busch Petra Beli Kathi Zarnack Julian König Jean-Yves Roignant Paul Lasko Makorin 1 controls embryonic patterning by alleviating Bruno1-mediated repression of oskar translation. PLoS Genetics |
author_facet |
Annabelle Dold Hong Han Niankun Liu Andrea Hildebrandt Mirko Brüggemann Cornelia Rücklé Heike Hänel Anke Busch Petra Beli Kathi Zarnack Julian König Jean-Yves Roignant Paul Lasko |
author_sort |
Annabelle Dold |
title |
Makorin 1 controls embryonic patterning by alleviating Bruno1-mediated repression of oskar translation. |
title_short |
Makorin 1 controls embryonic patterning by alleviating Bruno1-mediated repression of oskar translation. |
title_full |
Makorin 1 controls embryonic patterning by alleviating Bruno1-mediated repression of oskar translation. |
title_fullStr |
Makorin 1 controls embryonic patterning by alleviating Bruno1-mediated repression of oskar translation. |
title_full_unstemmed |
Makorin 1 controls embryonic patterning by alleviating Bruno1-mediated repression of oskar translation. |
title_sort |
makorin 1 controls embryonic patterning by alleviating bruno1-mediated repression of oskar translation. |
publisher |
Public Library of Science (PLoS) |
series |
PLoS Genetics |
issn |
1553-7390 1553-7404 |
publishDate |
2020-01-01 |
description |
Makorins are evolutionary conserved proteins that contain C3H-type zinc finger modules and a RING E3 ubiquitin ligase domain. In Drosophila, maternal Makorin 1 (Mkrn1) has been linked to embryonic patterning but the mechanism remained unsolved. Here, we show that Mkrn1 is essential for axis specification and pole plasm assembly by translational activation of oskar (osk). We demonstrate that Mkrn1 interacts with poly(A) binding protein (pAbp) and binds specifically to osk 3' UTR in a region adjacent to A-rich sequences. Using Drosophila S2R+ cultured cells we show that this binding site overlaps with a Bruno1 (Bru1) responsive element (BREs) that regulates osk translation. We observe increased association of the translational repressor Bru1 with osk mRNA upon depletion of Mkrn1, indicating that both proteins compete for osk binding. Consistently, reducing Bru1 dosage partially rescues viability and Osk protein level in ovaries from Mkrn1 females. We conclude that Mkrn1 controls embryonic patterning and germ cell formation by specifically activating osk translation, most likely by competing with Bru1 to bind to osk 3' UTR. |
url |
https://doi.org/10.1371/journal.pgen.1008581 |
work_keys_str_mv |
AT annabelledold makorin1controlsembryonicpatterningbyalleviatingbruno1mediatedrepressionofoskartranslation AT honghan makorin1controlsembryonicpatterningbyalleviatingbruno1mediatedrepressionofoskartranslation AT niankunliu makorin1controlsembryonicpatterningbyalleviatingbruno1mediatedrepressionofoskartranslation AT andreahildebrandt makorin1controlsembryonicpatterningbyalleviatingbruno1mediatedrepressionofoskartranslation AT mirkobruggemann makorin1controlsembryonicpatterningbyalleviatingbruno1mediatedrepressionofoskartranslation AT corneliaruckle makorin1controlsembryonicpatterningbyalleviatingbruno1mediatedrepressionofoskartranslation AT heikehanel makorin1controlsembryonicpatterningbyalleviatingbruno1mediatedrepressionofoskartranslation AT ankebusch makorin1controlsembryonicpatterningbyalleviatingbruno1mediatedrepressionofoskartranslation AT petrabeli makorin1controlsembryonicpatterningbyalleviatingbruno1mediatedrepressionofoskartranslation AT kathizarnack makorin1controlsembryonicpatterningbyalleviatingbruno1mediatedrepressionofoskartranslation AT juliankonig makorin1controlsembryonicpatterningbyalleviatingbruno1mediatedrepressionofoskartranslation AT jeanyvesroignant makorin1controlsembryonicpatterningbyalleviatingbruno1mediatedrepressionofoskartranslation AT paullasko makorin1controlsembryonicpatterningbyalleviatingbruno1mediatedrepressionofoskartranslation |
_version_ |
1714668730842087424 |